Wolfe, K. H._2001_Nat Rev Genet_Yesterday's polyploids and the mystery of diploidization

REVIEWS
No one would expect a 30-year-old book that is mostly about fish cytogenetics to be of much interest to mod-ern molecular biologists,particularly if that book had received lukewarm reviews at the time of publication 1,2.Nevertheless,citations of Susumu Ohno’s book Evolution by Gene Duplication 3have tripled between the years 1990 and 2000.In this book,written when only a few protein sequences were known,Ohno proposed that it is much easier to make new genes by duplicating old ones than to create them de novo ,and that genome duplication (polyploidy) was a quick and easy way to produce vast numbers of duplicate genes.Genome duplication could open the door to duplicating whole biochemical pathways.He famously proposed that two (or possibly three) rounds of polyploidy had occurred during the early evolution of the vertebrate lineage,but that further polyploidization then became impossible in mammals owing to the emergence of the X/Y sex-chro-mosome system.The human genome would thus be a paleopolyploid:an ancient polyploid that had later become diploid again,by means of sequence divergence between the duplicated chromosomes.
The renewed interest in Ohno’s ideas stems from two lines of research that began to bear fruit in the late 1980s.The first was what is now called comparative genomics.Genetic map comparisons among mammals confirmed that they contain large segments 4of con-served SYNTENY with conserved gene order.As early as 1973,Ohno had identified an apparently duplicated
chromosomal segment within the human genome,which was delineated by two pairs of duplicated genes on chromosomes 11 and 12 (REF.5).His proposal that these segments were remnants of ancient polyploidy (or some other form of ANEUPLOIDY ) meant that the develop-ment of comparative genetic maps between mam-malian genomes went hand-in-hand with a search for duplicated regions within them (for example,REF.6).The second line of research began with the discovery that the four HOX GENE CLUSTERS in mammals had evolved by quadruplication of a prototypic cluster similar to that of Drosophila .Schughart et al.7suggested that this quadruplication could have been associated with poly-ploidizations of the type envisaged by Ohno.Not only were the orders of the Hox genes in each cluster con-served between human and mouse,but also the gene order was essentially conserved among the four mam-malian clusters.The Hox clusters are a quadruplicated chromosomal segment.Subsequent discoveries of other duplicated genes that were linked to the Hox clusters indicated that the duplicated chromosomal regions might be quite large 8.
Ohno’s book was not very explicit about the number and timing of the proposed genome duplications,but the most widely accepted form of the hypothesis,which has been called the 2R hypothesis 9,is that there were two rounds of genome duplication in vertebrate ancestry:one immediately before,and one immediately after,the divergence of the lamprey lineage (see FIG.1and REF.10).
YESTERDAY’S POLYPLOIDS AND THE
MYSTERY OF DIPLOIDIZATION
Kenneth H.Wolfe
Thirty years after Susumu Ohno proposed that vertebrate genomes are degenerate polyploids,the extent to which genome duplication contributed to the evolution of the vertebrate genome,if at all, is still uncertain. Sequence-level studies on model organisms whose genomes show clearer evidence of ancient polyploidy are invaluable because they indicate what the evolutionary products of genome duplication can look like. The greatest mystery is the
molecular basis of diploidization, the evolutionary process by which a polyploid genome turns into a diploid one.
Smurfit Institute,Trinity College,University of
Dublin,Dublin 2,Republic of Ireland.e-mail:khwolfe@tcd.ie
proposes independent duplications of chromosomal segments and insertion of
nonsynonymous rate for all groups of
Vision and colleagues balance of
a single,
event,
65 Myr ago,
feature of
history.
other,
also occurred in
require more thorough analysis using phylogenetic trees and sequences from an
such as rice.。